Abstract
In this study we investigate the niche interaction between the frogs Physalameus cuvieri and Physalaemus kroyeri that occur in syntopy in water bodies of the Atlantic Forest located in the eastern Bahia State, Brazil. We investigated the niche width and overlap in the calling activity time, microhabitat use, diet composition, advertisement call, and body size. Both species preferred the same substrate and calling substrate categories, and showed low niche width values and high spatial niche overlap values. The pseudocommunity analysis revealed the absence of competition in space use. Ants and termites were the most important items in the diet of both species with the pseudocommunity analysis indicating an absence of competition in the diet. The two species demonstrate a greater similarity in body proportions and a high overlap in the calling activity time. However, they showed divergence in acoustic parameters, especially in the dominant frequency and call duration. Our results reinforce the role of advertisement call as a relevant attribute for anuran coexistence and highlight the importance of analyzing the various axes of the multidimensional niche for the most reliable description of the existence and magnitude of niche partitioning.
Key words
Advertisement call; diet; microhabitat use; niche partitioning
INTRODUCTION
The main objective of investigating interaction levels between species in an assemblage is to identify the drivers, causes, and effects that interaction exerts on diversity, hence providing the basis for understanding the mechanisms that regulate the coexistence between species (Losos 1996LOSOS JB. 1996. Phylogenetic perspectives on community ecology. Ecology 77: 1344-1354., Holt 2001HOLT RD. 2001. Species coexistence. Encycl Biodivers 5: 413-426.). In general, this research has focused on identifying the niche partitioning (structure) in the use of resources that involve a set of species from an assemblage (Arzabe et al. 1998ARZABE C, CARVALHO CX & COSTA MAG. 1998. Anurans assemblages in Crasto forest ponds (Sergipe State, Brazil): comparative structure and calling activity patters. Herpetol J 8: 111-113., Rossa-Feres & Jim 2001ROSSA-FERES DC & JIM J. 2001. Similaridade do sítio de vocalização em uma comunidade de anfíbios anuros na região noroeste do Estado de São Paulo, Brasil. Rev Bras Zool 18: 439-454., Leite-Filho et al. 2017LEITE-FILHO E, OLIVEIRA FA, ELOI FJ, LIBERAL CN, LOPES AO & MESQUITA DO. 2017. Evolutionary and ecological factors influencing an anuran community structure in an Atlantic Rainforest urban fragment. Copeia 105: 64-74.). However, the presence or magnitude of the phenomenon may be more evident between the pairs of phylogenetically close species (França et al. 2004FRANÇA LF, FACURE KG & GIARETTA AA. 2004. Trophic and spatial niches of two large-sized species of Leptodactylus (Anura) in southeastern Brazil. Stud Neotrop Fauna Environ 39: 243-248., Cajade et al. 2010CAJADE R, SCHAEFER EF, DURÉ MI & KEHR AI. 2010. Trophic and microhabitat niche overlap in two sympatric dendrobatids from La Selva, Costa Rica. Cuad Herpetol 24: 81-92., Jiménez & Bolaños 2012JIMÉNEZ R & BOLAÑOS F. 2012. Use of food and spatial resources by two frogs of the genus Dendropsophus (Anura: Hylidae) from La Selva, Costa Rica. Phyllomedusa 11: 51-62.), allowing for the development of several hypothesis tests on the effects of competition or evolutionary history on promoting the microevolutionary processes that play a relevant role in maintaining diversity (Webb et al. 2002WEBB CO, ACKERLY DD, MCPEEK MA & DONOGHUE MJ. 2002. Phylogenies and community ecology. Annu Rev Ecol Syst 33: 475-505., Losos 2008LOSOS JB. 2008. Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11: 995-1003.).
Winemiller et al. (2015)WINEMILLER KO, FITZGERALD DB, BOWER LM & PIANKA ER. 2015. Functional traits, convergent evolution, and periodic tables of niches. Ecol Lett 18: 737-751. highlighted that the spatial, trophic, life history, defense, and metabolic niche dimensions are the most relevant for measuring the interaction levels among species in an assemblage. In anurans, the spatial, trophic, and acoustic dimensions are considered as the most important for explaining the coexistence, and partition in the use of the habitat, microhabitat, prey composition or acoustic space has been often evidenced (Hödl 1977HÖDL W. 1977. Call differences and calling site segregation in anuran species from Central Amazonian floating meadows. Oecologia 28: 351-363., Lima & Magnusson 1998LIMA AP & MAGNUSSON WE. 1998. Partitioning seasonal time: interactions among size, foraging activity and diet in leaf-litter frogs. Oecologia 116: 259-266., Parmelee 1999PARMELEE JR. 1999. Trophic ecology of a tropical anuran assemblage. Sci Pap Nat Hist Museum Univ Kansas 11: 1-59., Sinsch et al. 2012SINSCH U, LÜMKEMANN K, ROSAR K, SCHWARZ C & DEHLING JM. 2012. Acoustic niche partitioning in an anuran community inhabiting an afromontane wetland (Butare, Rwanda). Afr Zool 47: 60-73.). Nevertheless, the richness and composition of species from an assemblage (Cardoso et al. 1989CARDOSO AJ, ANDRADE GV & HADDAD CFB. 1989. Distribuição espacial em comunidades de anfíbios (Anura) no Sudeste do Brasil. Rev Bras Biol 49: 241-249., Santos & Rossa-Feres 2007SANTOS TG & ROSSA-FERES DC. 2007. Similarities in calling site and advertisement call among anuran amphibians in southeastern Brazil. South Am J Herpetol 2: 17-30.), the complexity of the habitat (resource availability) (Bernarde & Anjos 1999BERNARDE PS & ANJOS L. 1999. Distribuição espacial e temporal da anurofauna no Parque Estadual Mata dos Godoy, Londrina, Paraná, Brasil (Amphibia: Anura). Comun Mus Ciênc Tecnol PUCRS Ser Zool 12: 127-140., Caldas et al. 2019CALDAS FLS, GARDA AA, CAVALCANTI LBQ, LEITE-FILHO E, FARIA RG & MESQUITA DO. 2019. Spatial and trophic structure of anuran assemblages in environments with different seasonal regimes in the brazilian Northeast region. Copeia 107: 567-584.), and the level of phylogenetic proximity between species (Protázio et al. 2015aPROTÁZIO AS, ALBUQUERQUE RL, FALKENBERG LM & MESQUITA DO. 2015a. Acoustic ecology of an anuran assemblage in the arid Caatinga of northeastern Brazil. J Nat Hist 49: 957-976., Caldas et al. 2019CALDAS FLS, GARDA AA, CAVALCANTI LBQ, LEITE-FILHO E, FARIA RG & MESQUITA DO. 2019. Spatial and trophic structure of anuran assemblages in environments with different seasonal regimes in the brazilian Northeast region. Copeia 107: 567-584.) can strongly affect the magnitude of resource partition among species.
In general, species with a close phylogenetic proximity are expected to have a high overlap in resource use because they have the same ecological and behavioral requirements due to their evolutionary linkage (Wiens et al. 2010WIENS JJ ET AL. 2010. Niche conservatism as an emerging principle in ecology and conservation biology. Ecol Lett 13: 1310-1324.). On the other hand, in saturated environments (high richness) and scarce resources, the pairs of phylogenetically close species may also show partitioning in some niche dimensions, thereby evidencing a niche complementarity (Santos & Rossa-Feres 2007SANTOS TG & ROSSA-FERES DC. 2007. Similarities in calling site and advertisement call among anuran amphibians in southeastern Brazil. South Am J Herpetol 2: 17-30., Sinsch et al. 2012SINSCH U, LÜMKEMANN K, ROSAR K, SCHWARZ C & DEHLING JM. 2012. Acoustic niche partitioning in an anuran community inhabiting an afromontane wetland (Butare, Rwanda). Afr Zool 47: 60-73., Protázio et al. 2019PROTÁZIO AS, PROTÁZIO AS & MESQUITA DO. 2019. Niche partitioning between two Physalaemus species (Anura, Leptodactylidae) in semiarid Caatinga in Northeast Brazil. North West J Zool 15: 157-167.). Thus, niche complementarity can reduce the negative effects of interaction because it decreases the overlap levels and increases the chances of coexistence (Schoener 1974SCHOENER TW. 1974. Resouce partitioning in ecological communities: research on how similar species divide resources helps reveal the natural regulation of species diversity. Science 185: 27-39.). Despite this, knowledge in terms of the way anurans share resources in assemblages has not yet been fully elucidated, which highlights the need for further investigations involving the different dimensions of the ecological niche for a more accurate interpretation of the mechanisms driving the phenomenon.
Physalaemus cuvieri and P. kroyeri (Figure 1) are two small frogs belonging to the Leptodactylidae family and Leiuperinae subfamily (Frost 2022FROST DR. 2022. Amphibians species of the world 6.1, an online reference.New York: America Museum of Natural History. https://amphibiansoftheworld.amnh.org/.
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). Physalaemus cuvieri has a wide distribution, present throughout the center and eastern Brazil and the eastern region of Paraguay, Argentina, and northern Uruguay (Lourenço et al. 2015LOURENÇO LB, TARGUETA CP, BALDO D, NASCIMENTO J, GARCIA PCA, ANDRADE GV, HADDAD CFB & RECCO-PIMENTEL SM. 2015. Phylogeny of frogs from the genus Physalaemus (Anura, Leptodactylidae) inferred from mitochondrial and nuclear gene sequences. Mol Phylogenet Evol 92: 204-216., Frost 2022FROST DR. 2022. Amphibians species of the world 6.1, an online reference.New York: America Museum of Natural History. https://amphibiansoftheworld.amnh.org/.
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). On the other hand, P. kroyeri has a more restricted distribution, being endemic to Brazil, and can be found in the north of the State of Minas Gerais and in the states of Bahia, Paraíba, Piauí, and Pernambuco (Lourenço et al. 2015LOURENÇO LB, TARGUETA CP, BALDO D, NASCIMENTO J, GARCIA PCA, ANDRADE GV, HADDAD CFB & RECCO-PIMENTEL SM. 2015. Phylogeny of frogs from the genus Physalaemus (Anura, Leptodactylidae) inferred from mitochondrial and nuclear gene sequences. Mol Phylogenet Evol 92: 204-216., Frost 2022FROST DR. 2022. Amphibians species of the world 6.1, an online reference.New York: America Museum of Natural History. https://amphibiansoftheworld.amnh.org/.
https://amphibiansoftheworld.amnh.org/...
). Both species belongs to the P. cuvieri species group, having as synapomorphy the persistence of ventrolateral gaps in the larval stage (Nascimento et al. 2005NASCIMENTO LB, CARAMASCHI U & CRUZ CAG. 2005. Taxonomic status review of the species groups of the genus Physalaemus Fitzinger, 1826 with revalidation of the genera Engystomops Jiménez-de-la-Espada, 1872 and Eupemphix Steindachner, 1863 (Amphibia, Anura, Leptodactylidae). Arq Mus Nac 63: 297-320., Vittorazzi et al. 2014VITTORAZZI SE, QUINDERÉ YRSD, RECCO-PIMENTEL SM, TOMATIS C, BALDO D, LIMA JRF, FERRO JM, LIMA JD & LOURENÇO LB. 2014. Comparative cytogenetics of Physalaemus albifrons and Physalaemus cuvieri species groups (Anura, Leptodactylidae). Comp Cytogenet 8: 103-124., Lourenço et al. 2015LOURENÇO LB, TARGUETA CP, BALDO D, NASCIMENTO J, GARCIA PCA, ANDRADE GV, HADDAD CFB & RECCO-PIMENTEL SM. 2015. Phylogeny of frogs from the genus Physalaemus (Anura, Leptodactylidae) inferred from mitochondrial and nuclear gene sequences. Mol Phylogenet Evol 92: 204-216.). In the adult phase, the two species show great behavioral, morphological, and ecological similarities using ponds, swamps, or lakes in open areas for breeding, with reproductive mode type 11 (Bokermann 1966BOKERMANN WCA. 1966. Notas sôbre tres espécies de “Physalaemus” de Maracás, Bahia. Rev Bras Biol 26: 253-259., Haddad & Prado 2005HADDAD CFB & PRADO CPA. 2005. Reproductive modes in frogs and their unexpected diversity in the Atlantic Forest of Brazil. BioScience 55: 207-217.).
The two species were found in syntopy in areas of Atlantic Forest in eastern Bahia State, showing a high overlap in the reproductive period, and also vocalizing synchronously in the same water bodies. Thus, they are excellent models for investigating how pairs of phylogenetically close species share resources involving different dimensions of the ecological niche. In this study, we investigated the niche relationship between syntopic populations of P. cuvieri and P. kroyeri in an area of the Atlantic Forest by analyzing the microhabitat use, prey composition, body size, advertisement call parameters, and calling activity time. Based on the hypothesis of niche partitioning involving some dimensions of the ecological niche, we aim to answer the following questions: (i) How do syntopic populations of P. cuvieri and P. kroyeri utilize resources in environments with high spatial (habitat) and temporal (reproductive period) overlap? (ii) Which dimensions of the multidimensional niche make coexistence between the two species possible?
MATERIALS AND METHODS
Study area
The study was conducted in Cruz das Almas municipality located in the eastern Bahia State, Northeast Brazil (Figure 2). Cruz das Almas is inserted in the Atlantic Forest Biome, in the region known as “Recôncavo Baiano,” characterized by its original vegetation of Seasonal Semideciduous Forest (Brazão & Araújo 1981BRAZÃO JEM & ARAÚJO AP. 1981. Vegetação. As regiões fitoecológicas, sua natureza e seus recursos econômicos. Estudo fitogeográfico. In: PROJETO RADAMBRASIL, Folha SD.24 Salvador. Geologia, Geomorfologia, Pedologia, Vegetação, Uso Potencial da Terra. Rio de Janeiro: Ministério das Minas e Energia, p. 405-464.). However, this vegetation was strongly reduced to small isolated fragments of secondary vegetation or large open areas for pasture and plantation. According to the Köppen classification, the climate is tropical monsoon (Am), with annual precipitation of 1,131.2 mm and an average temperature of 23.9 °C (Silva et al. 2016SILVA TSM, COELHO-FILHO MA & COELHO EF. 2016. Boletim meteorológico da estação convencional de Cruz das Almas, BA: variabilidade e tendências climáticas. Cruz das Almas: Embrapa Mandioca e Fruticultura, 77 p.).
Localization map of Cruz das Almas municipality showing the five-body water studied. PL – Permanent Lagoon; TP1 – Temporary Pond 1; TP2 – Temporary Pond 2; TP3 – Temporary Pond 3; TP4 – Temporary Pond 4.
Field activities were conducted from April 2015 to March 2019, totaling 20 sampling days. We sampled five different water bodies, where we observed individuals of P. cuvieri and P. kroyeri in simultaneous activity performed in the same space, evidencing a high temporal overlap:
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Temporary pond 1 (12°39’29’’S; 39°04’48’’W) – It is located in a region known as “Mata da Cascalheira”, a secondary forest habitat surrounded by cultivated areas and pasture. The ponds originate right after the rains from the formation of a temporary stream;
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Temporary pond 2 (12°39’35.5’’S; 39°05’37.7’’W) – It is formed at the edge of an experimental plantation of eucalyptus (Eucaliptus sp.). The puddle is located on the campus of the Federal University of Recôncavo da Bahia in a peri-urban environment, and is formed soon after the first rains. It lasts for about two weeks, after which it dries out completely;
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Temporary pond 3 (12°39’43.5’’S; 39°05’113.6’’W) – It is formed on the side of a road. The pond is also located in the field of the Federal University of Recôncavo da Bahia in a peri-urban environment. This pond forms right after the first rains and lasts for about two weeks, after which it dries up completely;
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Temporary pond 4 (12°40’24.5’’S; 39°04’15.6’’W) – It is located inside a forest fragment known as “Riacho do Machado”. The pond lies just below a hillside region having a predominance of medium-sized trees and shrubs;
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Permanente lagoon (12°39’36.8’’S; 39°04’41.8’’W) – It is located in the region known as “Mata da Cascalheira”. It is a body of water that is approximately 3 meters deep, with a predominance of reeds and macrophytes. The marginal vegetation comprises shrubs.
During field activities, other species engaged in the vocalization activity concomitant with those of P. cuvieri and P. kroyeri. Despite this, only Leptodactylus macrosternum was observed vocalizing in the same calling microhabitat used by P. cuvieri and P. kroyeri, but with a smaller number of individuals than the two Physalaemus. In addition, a single individual of the congener P. albifrons was also identified vocalizing together with P. cuvieri and P. kroyeri. However, because of the low sampling, P. albifrons was not included in our study.
Data collection
Field activities started at approximately 18:00 h and ended at 00:00 h, and were conducted by a minimum of three researchers. We used active and acoustic search to locate the individuals. All the collected specimens were euthanized with 2% lidocaine injection. They were then fixed with 10% formalin and stored in the Herpetological Collection of the Federal University of Recôncavo da Bahia (CHUFRB) (authorization SISBIO 46558-1 and 46558-2, and Ethics Committee on Animal Use of the Federal University of Recôncavo da Bahia – CEUA-UFRB 23007.007559/2016-71). In addition, we also analyzed the specimens of P. cuvieri and P. kroyeri housed at CHUFRB collected from the same study sites.
All individuals of P. cuvieri and P. kroyeri visualized had the used substrate (partially submerged, soil between vegetation, exposed soil, hole or emergent vegetation), the acoustic behavior (calling or silente), and the recording time registered for defining the spatial and temporal preference. We used the frequency data in each substrate category for calculating the spatial niche range using the inverse of Simpson’s (1949)SIMPSON EH. 1949. Measurement of diversity. Nature 163: 688. diversity index:
From this index, values ranging from 1 (specialist) to the total number of substrate categories identified (generalist) are generated. The niche overlap in substrate type was also calculated with Pianka’s (1973)PIANKA ER. 1973. The structure of lizard communities. Annu Rev Ecol Syst 4: 53-74. equation:
The overlap values range from 0 (no overlap) to 1 (complete overlap). Subsequently, a pseudocommunity analysis was performed for checking the presence of non-random patterns in the substrate type between the two species. The pseudocommunity analysis is based on a null model and creates expected patterns in the absence of competition. Thus, the average observed overlap was compared with the simulated average for checking the presence of non-random patterns (Gotelli & Graves 1996GOTELLI NJ & GRAVES GR. 1996. Null models in ecology. Washington: Smithsonia, 368 p.). The pseudocommunity analysis was performed in EcoSim 7.0 (Gotelli & Entsminger 2007GOTELLI NJ & ENTSMINGER GL. 2007. EcoSim: null models software for ecology. Acquired Intelligence Inc & Kesey-Bear. Jericho, VT 05465. http://garyentsminger.com/ecosim/.
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), using the type 2 randomization algorithm (RA2) with 1000 randomizations. Because reproductive males of anurans may show specificity for calling microhabitat, we also studied the relationship between calling males of P. cuvieri and P. kroyeri. We evaluated whether males exhibited partitioning in the calling substrate type to reduce the competition levels and allow for reproductive success, using the same parameters described above.
For the diet analysis, stomachs and intestines were removed by incision in the ventral region of the individuals (Parmelee 1999PARMELEE JR. 1999. Trophic ecology of a tropical anuran assemblage. Sci Pap Nat Hist Museum Univ Kansas 11: 1-59.). Additionally, we also used stomach flushing for diet analysis, by following the protocol described by Solé et al. (2005)SOLÉ M, BECKMANN O, PELZ B, KWET A & ENGELS W. 2005. Stomach-flushing for diet analysis in anurans: an improved protocol evaluated in a case study in Araucaria forests, southern Brazil. Stud Neotrop Fauna Environ 40: 23-28.. The food items were then analyzed in a Petri dish and observed under an Olympus SZ51 stereomicroscope. All items were identified to the taxonomic level of order, except ants, considered a separate prey category of Hymenoptera. All prey found in the gastrointestinal tracts were counted per individual to determine the numerical frequency (NF%). The prey that was intact had their length and width measured with digital calipers (accurate up to 0.01 mm) to establish the volumetric frequency (VF%), estimated using the ellipsoid formula:
Subsequently, the frequency of occurrence of prey category (OF%) was defined from the ratio between the total number of gastrointestinal tracts with prey category i divided by the total number of gastrointestinal tracts analyzed. Then, the relevant items in the diet of P. cuvieri and P. kroyeri were determined by calculating the importance index of each prey category using the formula:
Finally, we calculated the niche width in the diet, food niche overlap, and performed a pseudocommunity analysis to check the presence of competition in the trophic niche using the same parameters described for the substrate type.
In total, 11 morphometric variables were measured using digital calipers (precision of 0.01 mm) and a stereomicroscope, following Napoli & Pimenta (2009)NAPOLI MF & PIMENTA BVS. 2009. A new species of the Bokermannohyla circumdata group (Anura: Hylidae) from the coastal forests of Bahia, northeastern Brazil. Copeia 2009: 674-683.: snout-vent length (SVL); head length (HL); head width (HW); eye-nostril distance (END); internarial distance (ID); intereye distance (IED); thigh length (THL); tibia length (TL); foot length (FL); tympanum diameter (TD); and eye diameter (ED). All morphometric variables were logarithmically transformed (Log10) to obtain normality. The effect size generated by isometric variation was reduced by the linear regression residuals by the creation of a “body size” variable, which represented the total partition of the variation in the size and shape of each individual (Somers 1986SOMERS KM. 1986. Multivariate allometry and removal of size with principal component analysis. Syst Zool 35: 359-368.). Body size values were obtained from the equation p−0.5, where p is the number of measured variables (Jolicoeur 1963JOLICOEUR P. 1963. The multivariate generalization of the allometry equation. Biometrics 19: 497-499.) multiplied by the sum of all the observations. The body size variable was subsequently used to perform simple regressions against the other morphometric variables and the generated residuals were retained. These residuals were used to create a new covariance matrix of the adjusted variables from the Principal Component Analysis. Simple regressions and Principal Component Analyses were conducted with the Past 4.01 software (Hammer et al. 2009HAMMER Ø, HAPER DAT & RYAN PD. 2009. Past: paleontological statistics software package for education and data analysis. Palaeontol Electron 4: 1-9.).
The advertisement call of P. cuvieri and P. kroyeri were recorded with a Tascam DR-05X recorder coupled to a Yoga HT-320 unidirectional microphone at approximately 1 m of distance from the calling males, with a sampling rate of 44100 Hz and 16 bits of resolution. For each male recorded, a track of one-minute was analyzed in the program Raven Pro 1.5 (Lab of Ornithology, Cornell University), and produced spectrograms using the Discrete Fourier Transformation, with 256 samples, overlap 50%, Hann window type and window width 256. In the acoustic analysis, spectral parameters were obtained from the spectrograms, whereas temporal parameters were obtained from the oscillograms. We measured five acoustic parameters, following the definitions of Köhler et al. (2017)KÖHLER J, JANSEN M, RODRÍGUEZ A, KOK PJR, TOLEDO LF, EMMRICH M, GLAW F, HADDAD CFB, RÖDEL MO & VENCES M. 2017. The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa 4251: 1-124.: call duration (s), distance between call (s), call repetition rate (call/second), fundamental frequency (Hz), and dominant frequency (Hz). We followed the acoustic nomenclature of Hepp & Pombal (2020)HEPP F & POMBAL JP. 2020. Review of bioacoustical traits in the genus Physalaemus Fitzinger, 1826 (Anura: Leptodactylidae: Leiuperinae). Zootaxa 4725: 1-106., who considered the advertisement call of the two species to be a continuous whine-like emission, nonpulsed, and having the presence of harmonics with downward frequency modulation at the beginning of the call and up-downward at the half or end.
Subsequently, we used the Kernel density function to calculate the distribution estimate of the advertisement call parameters between the two species. The Kernel density estimator is a nonparametric estimator used for continuous data with unknown distribution (Geange et al. 2011GEANGE SW, PLEDGER S, BURNS KC & SHIMA JS. 2011. A unified analysis of niche overlap incorporating data of different types. Methods Ecol Evol 2: 175-184.). In addition, we performed a permutation test of equality using 1000 randomizations with bootstrap. We also used the Kernel density function to calculate the estimated temporal distribution of the calling males, using the time of the acoustic report as descriptor. Additionally, Mann-Whitney U test was used to verify diferences in acoustic parameters of the advertisement call. The Kernel density estimation was performed in R software (R Core Team 2019)R CORE TEAM. 2019. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
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, using the sm.density.compare function of the “sm” package (Bowman & Azzalini 2019BOWMAN A & AZZALINI A. 2019. “sm”: Smoothing Methods for Nonparametric Regression and Density Estimation. R package version 2.2 - 5.6. https://cran.r-project.org/web/packages/sm/.
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), whereas the Mann-Whitney U test was performed in Past 4.01 software (Hammer et al. 2009HAMMER Ø, HAPER DAT & RYAN PD. 2009. Past: paleontological statistics software package for education and data analysis. Palaeontol Electron 4: 1-9.).
RESULTS
Physalaemus cuvieri used four categories of substrate, whereas P. kroyeri used five substrate categories. Both species showed a preference for partially submerged substrate (Figure 3). The values and niche width of substrate type were low and similar between the two species (P. cuvieri: 1.49; P. kroyeri: 1.51). Calling males of both species showed a preference for vocalizing while staying partially submerged, indicating specialization on the calling substrate (P. cuvieri: 1.04; P. kroyeri: 1.00). Both species showed a high overlap in substrate (0.99) and calling substrate (1.0). For the substrate, the pseudocommunity analysis revealed an observed mean of 0.99 and a simulated mean of 0.69, with the chance of the observed mean being lower than the expected mean not significant (p = 0.99), thereby indicating no competition. For the calling substrate, the pseudocommunity analysis revealed an observed mean of 1.0 and a simulated mean of 0.65, with the chance of the observed mean being less than expected also not significant (p = 0.99).
Substrate and calling substrate of Physalaemus cuvieri and Physalaemus kroyeri. PS: Partially submerged; SBV: Soil between vegetation; ES: Exposed soil; HOL: Hole; EV: Emergent vegetation. The value above bars represents the number of individuals. NB: niche breadth; NBcalling: niche breadth of the calling substrate.
In the diet of P. cuvieri, eight prey categories were found. The most important items were ants (58.12) and termites (40.20) (Table I), whereas in the diet of P. kroyeri, seven prey categories were found with the most important items being termites (51.25) and ants (46.50). Numerical and volumetric niche width values were similar, with P. cuvieri (numeric breadth: 1.75) having numerical niche width values slightly higher than P. kroyeri (numeric breadth: 1.27). The overlap analysis revealed an average observed overlap of 0.92 and a simulated overlap of 0.51. The pseudocommunity analysis showed no competition in the food niche (p = 1.0). Because of the poor adjustment in the dispersion of the analyzed number of items per stomach (P. cuvieri: 4.77 ± 5.79; P. kroyeri: 7.22 ± 13.3), we refined our analysis by removing the effects of individuals that displayed as outliers (one P. cuvieri and three P. kroyeri). The new adjusted analysis promoted a better adjustment of the data for number of items per stomach (P. cuvieri: 3.25 ± 1.96; P. kroyeri: 2.35 ± 2.16) and revealed that the numerical and volumetric niche width values remained similar to the values of the previous analysis (P. cuvieri: numeric breadth = 1.68, volumetric breadth = 1.00; P. kroyeri: numeric breadth = 1.28, volumetric breadth = 1.0). Ants and termites were the most important preys in the diet of both species (P. cuvieri: 60.08, 33.33; P. kroyeri: 86.39, 3.19, respectively).
Diets of Physalaemus cuvieri and Physalaemus kroyeri in Cruz das Almas municipality, Bahia State. N = numerical frequency, V = volumetric frequency, F = occurrence frequency, I = importance index.
Physalaemus cuvieri (28.8 mm) showed a greater snout-vent length than P. kroyeri (22.9 mm) (Table II). The Principal Component Analysis revealed that the first and second components (PC) explained 59.11% of the variation in the data set. PC1 was positively influenced by the internarial distance and intereye distance and was negatively affected by tympanum diameter and foot length. However, PC2 was positively affected by tympanum diameter and intereye distance and negatively influenced by eye-nostril distance and eye diameter. Nevertheless, the observation of loadings and scatter plot revealed that P. cuvieri and P. kroyeri occupy the same morphometric space, evidencing a strong similarity in body proportions (Figure 4).
Axes I and II of the Principal Components Analysis based on adjusted morphometric data for Physalaemus cuvieri and P. kroyeri from Cruz das Almas, Bahia State, Brazil.
Morphometric variables (mm) and Principal Component Analysis (PCA) of 11 morphometric variables of Physalaemus cuvieri and Physalaemus kroyeri from Cruz das Almas municipality, Bahia State, Brazil. Values above parentheses represent mean ± standard deviation. Values in the parentheses represent the minimum and maximum. In PCA, the variables are adjusted.
The advertisement call of both species was formed by a single note (Figure 5). Physalaemus cuvieri showed a shorter advertisement call (0.297 ± 0.029 s) and shorter intercall interval (2.085 ± 2.067 s) than P. kroyeri (0.761 ± 0.076 s and 9.018 ± 4.814 s, respectively) (Table III). The advertisement calls had many harmonics and displayed a general downward frequency modulation at the beginning of the call. In P. cuvieri, most of the call energy was in the first harmonic, while in P. kroyeri most of the call energy was concentrated between the fourth and seventh harmonics. Subharmonics were present in the initial third of the advertisement call of P. cuvieri. The dominant frequency of P. cuvieri was lower (755.98 ± 68.36 Hz) than that of P. kroyeri (2,748 ± 228.23 Hz), and the fundamental frequency of P. kroyeri (539.6 ± 37.66 Hz) was lower than that of P. cuvieri (755.98 ± 68.36 Hz). The Kernel density analysis and the Mann-Whitney U test revealed differences in all parameters of the advertisement call, notably in call duration and dominant frequency, thus indicating partitioning in the acoustic niche (Table III, Figure 6). Contrarily, the analysis of the calling activity time of the males indicated a high overlap and lack of partition in the temporal niche.
Advertisement call parameters of Physalaemus cuvieri and Physalaemus kroyeri. a–b: Oscillogram; c–d: Spectrogram; e–f: Power spectrum showing the dominant frequencies.
Plot of Kernel density estimate showing the acoustic space occupied for Physalaemus cuvieri and Physalaemus kroyeri. p is result of the permutation test of equality with 1000 randomization (bootstrap). Bandwidth (bw) is the mean of the optimal values for the normal distribution of the two groups.
DISCUSSION
In this study, P. cuvieri and P. kroyeri showed a high temporal, spatial, and feeding overlap, but a low acoustic overlap, thereby indicating that acoustic niche partitioning is relevant for the coexistence between the two leptodactylids. Many researchers have reported the existence of acoustic partitioning among anurans (Bourne & York 2001BOURNE GR & YORK H. 2001. Vocal behaviors are related to nonrandom structure of anuran breeding assemblages in Guyana. Ethol Ecol Evol 13: 313-329., Martins & Jim 2003MARTINS IA & JIM J. 2003. Bioacoustic analysis of advertisement call in Hyla nana and Hyla sanborni (Anura, Hylidae) in Botucatu, São Paulo, Brazil. Braz J Biol 63: 507-516., Santos & Rossa-Feres 2007SANTOS TG & ROSSA-FERES DC. 2007. Similarities in calling site and advertisement call among anuran amphibians in southeastern Brazil. South Am J Herpetol 2: 17-30., Silva et al. 2008SILVA RA, MARTINS IA & ROSSA-FERES DC. 2008. Bioacústica e sítio de vocalização em taxocenoses de anuros de área aberta no noroeste paulista. Biota Neotrop 8: 123-134., Protázio et al. 2015aPROTÁZIO AS, ALBUQUERQUE RL, FALKENBERG LM & MESQUITA DO. 2015a. Acoustic ecology of an anuran assemblage in the arid Caatinga of northeastern Brazil. J Nat Hist 49: 957-976., Bignotte-Giró et al. 2019BIGNOTTE-GIRÓ I, FONG A & LÓPEZ-IBORRA GM. 2019. Acoustic niche partitioning in five Cuban frogs of the genus Eleutherodactylus. Amphib-Reptil 40: 1-11.), and it appears to be a much more common phenomenon than has been reported. However, previous studies that have shown the existence of acoustic partitioning among anurans have focused on the exclusive investigation of the interaction in the acoustic space, without considering the other niche dimensions (Duellman & Pyles 1983DUELLMAN WE & PYLES RA. 1983. Acoustic resource partitioning in anuran communities. Copeia 3: 639-649., Márquez et al. 1993MÁRQUEZ R, DE LA RIVA I & BOSCH J. 1993. Advertisement calls of Bolivian species of Hyla (Amphibia, Anura, Hylidae). Biotropica 25: 426-443., Pombal 2010POMBAL JP. 2010. O espaço acústico em uma taxocenose de anuros (Amphibia) do sudeste do Brasil. Arq Mus Nac 68: 135-144., Lima et al. 2019LIMA MSCS, PEDERASSI J, PINESCHI RB & BARBOSA DBS. 2019. Acoustic niche partitioning in an anuran community from the municipality of Floriano, Piauí, Brazil. Braz J Biol 79: 566-576.), which may mask the real magnitude of the interaction and the dynamics of resource use across the different axes of the multidimensional niche.
On the other hand, it is possible that partitioning is reflected in other microhabitat descriptors, which help in reducing the overlap levels (Rossa-Feres & Jim 2001ROSSA-FERES DC & JIM J. 2001. Similaridade do sítio de vocalização em uma comunidade de anfíbios anuros na região noroeste do Estado de São Paulo, Brasil. Rev Bras Zool 18: 439-454., Silva et al. 2008SILVA RA, MARTINS IA & ROSSA-FERES DC. 2008. Bioacústica e sítio de vocalização em taxocenoses de anuros de área aberta no noroeste paulista. Biota Neotrop 8: 123-134.). Protázio et al. (2019)PROTÁZIO AS, PROTÁZIO AS & MESQUITA DO. 2019. Niche partitioning between two Physalaemus species (Anura, Leptodactylidae) in semiarid Caatinga in Northeast Brazil. North West J Zool 15: 157-167. studied the niche interaction between two other Physalaemus species (P. albifrons and Physalaemus cicada) in the Caatinga of northeastern Brazil and identified differences in the distance to the pond edge and the in depth of the water column used by the two species. However, P. albifrons and P. cicada are not very similar in morphology, calls and behavior, which may explain the result found by the authors. A similar result was found in Argentina by Duré & Kehr (2004)DURÉ MI & KEHR AI. 2004. Influence of microhabitat on the trophic ecology of two leptodactylids from northeastern Argentina. Herpetologica 60: 295-303. who found that Leptodactylus latinasus prefer mud near ponds, whereas Leptodactylus bufonius preferred dry land, suggesting that partition identification may be associated with the scale of analysis and involve other descriptors of the spatial niche. In our study, only the advertisement call showed differences between the two species, reinforcing the role of the advertisement call as an important trait of niche interation.
In general, a negative relationship seems to exist between spatial niche overlap and acoustic niche overlap. Species with a high overlap in the acoustic space tend to show a low overlap in the spatial dimensions, whereas species with a high spatial overlap tend to show acoustic partitioning (Silva et al. 2008SILVA RA, MARTINS IA & ROSSA-FERES DC. 2008. Bioacústica e sítio de vocalização em taxocenoses de anuros de área aberta no noroeste paulista. Biota Neotrop 8: 123-134., Tárano 2010TÁRANO Z. 2010. Advertisement calls and calling habits of frogs from a flooded savanna of Venezuela. South Am J Herpetol 5: 221-240., Abrunhosa et al. 2014ABRUNHOSA PA, WOGEL H & POMBAL JP. 2014. Spatial and temporal organization in three syntopic species of the Scinax ruber group (Anura: Hylidae) in the Atlantic rainforest, southeastern Brazil. J Nat Hist 48: 2449-2471., Protázio et al. 2015aPROTÁZIO AS, ALBUQUERQUE RL, FALKENBERG LM & MESQUITA DO. 2015a. Acoustic ecology of an anuran assemblage in the arid Caatinga of northeastern Brazil. J Nat Hist 49: 957-976.). This can drive to the interpretation of primary importance of space in the niche interaction (Cunha & Vieira 2004CUNHA AA & VIEIRA MV. 2004. Two bodies cannot occupy the same place at the same time, or the importance of space in the ecological niche. Bull Ecol Soc Am 85: 25-26.). However, our results reinforce the importance of the acoustic niche as a relevant ecological attribute in the interaction. We believe that in interactions involving closely related and sympatric species with acoustic communication, the acoustic dimension is more important than the spatial dimension. Because habitat and microhabitat use of anurans can be regulated by phylogenetic constraints (Zimmerman & Simberloff 1996ZIMMERMAN BL & SIMBERLOFF D. 1996. An historical interpretation of habitat use by frogs in a Central Amazonian forest. J Biogeogr 23: 27-46.), the high overlap in microhabitat use between the two Physalaemus species suggests a strong historical influence in the space use. Physalaemus cuvieri and P. kroyeri have type 11 reproductive mode with the development of exotrophic tadpole in foam nests (Haddad & Prado 2005HADDAD CFB & PRADO CPA. 2005. Reproductive modes in frogs and their unexpected diversity in the Atlantic Forest of Brazil. BioScience 55: 207-217.). Hence, they must have the same behavioral and physiological requirements reflected in the preference for specific microhabitat (Ernst & Rödel 2006ERNST R & RÖDEL MO. 2006. Community assembly and structure of tropical leaf-litter anurans. Ecotropica 12: 113-129.). This may explain the high values of overlap observed in substrate and calling substrate.
Anurans are often considered opportunistic predators, and their feeding may vary according to the availability of prey in the environment (Ceron et al. 2019CERON K, OLIVEIRA-SANTOS LGR, SOUZA CS, MESQUITA DO, CALDAS FLS, ARAUJO AC & SANTANA DJ. 2019. Global patterns in anuran–prey networks: structure mediated by latitude. Oikos 128: 1537-1548.). However, there is evidence of species that have preferential prey categories, which indicates different levels of specialization (Toft 1985TOFT CA. 1985. Resource partitioning in amphibians and reptiles. Copeia 1985: 1-21.). Yet, the feeding pattern observed in P. cuvieri and P. kroyeri suggests that both species exhibit an active foraging behavior, with direct search for food items (Parmelee 1999PARMELEE JR. 1999. Trophic ecology of a tropical anuran assemblage. Sci Pap Nat Hist Museum Univ Kansas 11: 1-59.) that explains the striking coincidence of the presence of termites and ants as the most important items in the diet of both species. Other authors have also reported the presence of termites and ants as relevant items in the diet of other species of the genus Physalaemus in different biomes (e.g., P. albifrons, Protázio et al. 2019PROTÁZIO AS, PROTÁZIO AS & MESQUITA DO. 2019. Niche partitioning between two Physalaemus species (Anura, Leptodactylidae) in semiarid Caatinga in Northeast Brazil. North West J Zool 15: 157-167.; Physalaemus biligonigerus, Oliveira et al. 2015OLIVEIRA M, GOTTSCHALK MS, LOEBMANN D, SANTOS MB, MIRANDA S, ROSA C & TOZETTI AM. 2015. Diet composition and niche overlap in two sympatric species of Physalaemus (Anura, Leptodactylidae, Leiuperinae) in coastal subtemperate wetlands. Herpetol Notes 8: 173-177.; Physalaemus centralis, Marques-Pinto et al. 2019MARQUES-PINTO T, BARRETO-LIMA AF & BRANDÃO RA. 2019. Dietary resource use by an assemblage of terrestrial frogs from the Brazilian Cerrado. North West J Zool 15: 135-146.; P. cicada, Santana & Juncá 2007SANTANA AS & JUNCÁ FA. 2007. Diet of Physalaemus cf. cicada (Leptodactylidae) and Bufo granulosus (Bufonidae) in a semideciduous forest. Braz J Biol 67: 125-131., Leite-Filho et al. 2015LEITE-FILHO E, VIEIRA WLS, SANTANA GG, ELOI FJ & MESQUITA DO. 2015. Structure of a Caatinga anuran assemblage in Northeastern Brazil. Neotrop Biol Conserv 10: 63-73.; P. cuvieri, Santos et al. 2004SANTOS EM, ALMEIDA AV & VASCONCELOS SD. 2004. Feeding habits of six anuran (Amphibia: Anura) species in a rainforest fragment in northeastern Brazil. Iheringia 94: 433-438., Leivas et al. 2018LEIVAS PT, LEIVAS FWT & CAMPIÃO K. 2018. Diet and parasites of the anuran Physalaemus cuvieri Fitzinger, 1826 (Leiuperidae) from an Atlantic Forest fragment. Herpetol Notes 11: 109-113., Caldas et al. 2019CALDAS FLS, GARDA AA, CAVALCANTI LBQ, LEITE-FILHO E, FARIA RG & MESQUITA DO. 2019. Spatial and trophic structure of anuran assemblages in environments with different seasonal regimes in the brazilian Northeast region. Copeia 107: 567-584.; Physalaemus gracilis, Moser et al. 2017MOSER CF, AVILA FR, OLIVEIRA M & TOZETTI AM. 2017. Diet composition and trophic niche overlap between two sympatric species of Physalaemus (Anura, Leptodactylidae, Leiuperinae) in a subtemperate forest of southern Brazil. Herpetol Notes 10: 9-15.; Physalaemus lisei, Moser et al. 2017MOSER CF, AVILA FR, OLIVEIRA M & TOZETTI AM. 2017. Diet composition and trophic niche overlap between two sympatric species of Physalaemus (Anura, Leptodactylidae, Leiuperinae) in a subtemperate forest of southern Brazil. Herpetol Notes 10: 9-15.), driving to the existence of a strong historical influence in the diet of the clade’s species (Protázio et al. 2015bPROTÁZIO AS, ALBUQUERQUE RL, FALKENBERG LM & MESQUITA DO. 2015b. Niche differentiation of an anuran assemblage in temporary ponds in the brazilian semiarid Caatinga: influence of ecological and historical factors. Herpetol J 25: 109-121., Leivas et al. 2018LEIVAS PT, LEIVAS FWT & CAMPIÃO K. 2018. Diet and parasites of the anuran Physalaemus cuvieri Fitzinger, 1826 (Leiuperidae) from an Atlantic Forest fragment. Herpetol Notes 11: 109-113.).
However, there are previous research that showed the opposite, and evidenced the existence of food partition between pairs of species of the genus Physalaemus, as well as preference for prey categories other than termites and ants (Oliveira et al. 2015OLIVEIRA M, GOTTSCHALK MS, LOEBMANN D, SANTOS MB, MIRANDA S, ROSA C & TOZETTI AM. 2015. Diet composition and niche overlap in two sympatric species of Physalaemus (Anura, Leptodactylidae, Leiuperinae) in coastal subtemperate wetlands. Herpetol Notes 8: 173-177., Protázio et al. 2019PROTÁZIO AS, PROTÁZIO AS & MESQUITA DO. 2019. Niche partitioning between two Physalaemus species (Anura, Leptodactylidae) in semiarid Caatinga in Northeast Brazil. North West J Zool 15: 157-167.). These findings suggests that behavioral (foraging behavior) and ecological factors (competition, predation risk, and prey availability) also strongly influence the interaction of different species of the clade in the food niche (Perry & Pianka 1997PERRY G & PIANKA ER. 1997. Animal foraging: past, present and future. Trends Ecol Evol 12: 360-364.). Thus, the pattern in the food niche interaction observed between P. cuvieri and P. kroyeri from Cruz das Almas municipality may be peculiar to the study site, resulting from historical processes that operated in the community over a spatiotemporal scale (evolution, chances, dispersal limit, biotic, and abiotic filters) (Hillerislambers et al. 2012HILLERISLAMBERS J, ADLER PB, HARPOLE WS, LEVINE JM & MAYFIELD MM. 2012. Rethinking community assembly through the lens of coexistence theory. Annu Rev Ecol Evol Syst 43: 227-248.).
The evidence of acoustic partitioning observed between the two species strengthens the importance of advertisement call as a relevant attribute in the niche relationship and appears to be sufficient for ensuring the coexistence of the two Physalaemus. The differentiation in the advertisement call between the pairs of anuran species is recognized as relevant to avoid hybridization and ensure reproductive isolation (Fouquette 1960FOUQUETTE MJ. 1960. Isolating mechanisms in three sympatric treefrogs in the Canal Zone. Evolution 14: 484-497.). Because the advertisement call presents a strong phylogenetic signal (Ryan & Rand 1999RYAN MJ & RAND AS. 1999. Phylogenetic influence on mating call preferences in female tungara frogs, Physalaemus pustulosus. Anim Behav 57: 945-956., Erdtmann & Amézquita 2009ERDTMANN L & AMÉZQUITA A. 2009. Differential evolution of advertisement call traits in dart-poison frogs (Anura: Dendrobatidae). Ethology 115: 801-811.), the divergence in acoustic traits between the pairs of closely related and sympatric species can be interpreted as a shift of reproductive character (Blair 1974BLAIR WF. 1974. Character displacement in frogs. Am Zool 14: 1119-1125., Gerhardt 1994aGERHARDT HC. 1994a. Repruductive character displacement of female mate choice in the grey treefrog, Hyla chrysoscelis. Anim Behav 47: 959-969.). Thus, variations in the parameters of advertisement call appear to reflect an evolutionary adjustment of the signal as an attempt to avoid or reduce acoustic interference from neighboring heterospecific males (Chek et al. 2003CHEK AA, BOGART JP & LOUGHEED SC. 2003. Mating signal partitioning in multi-species assemblages: a null model test using frogs. Ecol Lett 6: 235-247.).
Acoustic partitioning among anuran species appear to be reflected in divergences in the dominant frequency and in the call duration of species that present a high spatial and temporal overlap, as observed by Salas et al. (1998)SALAS NE, ZAVATTIERI MV, TADA IED, MARTINO AL & BRIDAROLLI ME. 1998. Bioacoustical and etho-ecological features in amphibian communities of Southern Cordoba Province (Argentina). Cuad Herpetol 12: 37-46.. This result agrees with our findings: P. cuvieri and P. kroyeri showed a marked differentiation in the call duration and dominant frequency. Dominant frequency is considered a static acoustic trait, shaped by stabilizing selection, and with an important role in the species recognition, in the reproductive isolation and sexual selection (Gerhardt 1994bGERHARDT HC. 1994b. The evolution vocalization in frogs and toads. Annu Rev Ecol Syst 25: 293-324., Nityananda & Bee 2011NITYANANDA V & BEE MA. 2011. Finding your mate at a cocktail party: frequency separation promotes auditory stream segregation of concurrent voices in multi-species frog choruses. PLoS One 6: 1-11.), whereas call duration plays an important role in female preference and also sexual selection (Wilczynski et al. 1999WILCZYNSKI W, RAND AS & RYAN MJ. 1999. Female preferences for temporal order of call components in the tungara frog: a Bayesian analysis. Anim Behav 58: 841-851., Gerhardt & Brooks 2009GERHARDT HC & BROOKS R. 2009. Experimental analysis of multivariate female choice in gray treefrogs (Hyla versicolor): evidence for directional and stabilizing selection. Evolution 63: 2504-2512.). Thus, the acoustic divergence observed between P. cuvieri and P. kroyeri may allow both the recognition of males by the female and the selection of those with the best fitness.
Finally, partitioning in the acoustic signal can operate by involving multimodal channels, with a synergy of several biological aspects that not only involve interaction (Gerhardt 1994bGERHARDT HC. 1994b. The evolution vocalization in frogs and toads. Annu Rev Ecol Syst 25: 293-324.). For example, males can alter their position to improve the reception of a specific signal or even alter the timing of their call to avoid temporal overlap (Schwartz & Wells 1983SCHWARTZ JJ & WELLS KD. 1983. An experimental study of acoustic interference between two species of neotropical treefrogs. Anim Behav 31: 181-190., Chek et al. 2003CHEK AA, BOGART JP & LOUGHEED SC. 2003. Mating signal partitioning in multi-species assemblages: a null model test using frogs. Ecol Lett 6: 235-247.). Thus, we believe that the acoustic partitioning observed between P. cuvieri and P. kroyeri may involve other aspects of the advertisement call of both species. However, approaches considering the varying degrees of different ecological traits of sympatric and allopatric populations of the two species may help define the real importance of the advertisement call in the interaction. Our results reveal that acoustic niche partitioning is an important mechanism of niche segregation, and seems to be of primary importance to avoid hybridization and reduce competition for food and space, ensuring co-occurrence of the two species in the studied ponds.
ACKNOWLEDGMENTS
We thank Amanda C. Caldas, Diego Macedo, Lucas S. Nascimento and Ubiraci C. Reis Jr. for their help with the field work and ICMBio for granting the collecting permit.
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Publication Dates
-
Publication in this collection
14 Apr 2023 -
Date of issue
2023
History
-
Received
06 Oct 2021 -
Accepted
28 Apr 2022